IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-38575-6.html
   My bibliography  Save this article

Homeostatic synaptic plasticity rescues neural coding reliability

Author

Listed:
  • Eyal Rozenfeld

    (Tel Aviv University
    Tel Aviv University)

  • Nadine Ehmann

    (Leipzig University)

  • Julia E. Manoim

    (Tel Aviv University)

  • Robert J. Kittel

    (Leipzig University)

  • Moshe Parnas

    (Tel Aviv University
    Tel Aviv University)

Abstract

To survive, animals must recognize reoccurring stimuli. This necessitates a reliable stimulus representation by the neural code. While synaptic transmission underlies the propagation of neural codes, it is unclear how synaptic plasticity can maintain coding reliability. By studying the olfactory system of Drosophila melanogaster, we aimed to obtain a deeper mechanistic understanding of how synaptic function shapes neural coding in the live, behaving animal. We show that the properties of the active zone (AZ), the presynaptic site of neurotransmitter release, are critical for generating a reliable neural code. Reducing neurotransmitter release probability of olfactory sensory neurons disrupts both neural coding and behavioral reliability. Strikingly, a target-specific homeostatic increase of AZ numbers rescues these defects within a day. These findings demonstrate an important role for synaptic plasticity in maintaining neural coding reliability and are of pathophysiological interest by uncovering an elegant mechanism through which the neural circuitry can counterbalance perturbations.

Suggested Citation

  • Eyal Rozenfeld & Nadine Ehmann & Julia E. Manoim & Robert J. Kittel & Moshe Parnas, 2023. "Homeostatic synaptic plasticity rescues neural coding reliability," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-38575-6
    DOI: 10.1038/s41467-023-38575-6
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-38575-6
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-38575-6?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Atefeh Pooryasin & Marta Maglione & Marco Schubert & Tanja Matkovic-Rachid & Sayed-mohammad Hasheminasab & Ulrike Pech & André Fiala & Thorsten Mielke & Stephan J. Sigrist, 2021. "Unc13A and Unc13B contribute to the decoding of distinct sensory information in Drosophila," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    2. Eyal Rozenfeld & Merav Tauber & Yair Ben-Chaim & Moshe Parnas, 2021. "GPCR voltage dependence controls neuronal plasticity and behavior," Nature Communications, Nature, vol. 12(1), pages 1-11, December.
    3. Georg Dietzl & Doris Chen & Frank Schnorrer & Kuan-Chung Su & Yulia Barinova & Michaela Fellner & Beate Gasser & Kaolin Kinsey & Silvia Oppel & Susanne Scheiblauer & Africa Couto & Vincent Marra & Kry, 2007. "A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila," Nature, Nature, vol. 448(7150), pages 151-156, July.
    4. Shawn R. Olsen & Rachel I. Wilson, 2008. "Lateral presynaptic inhibition mediates gain control in an olfactory circuit," Nature, Nature, vol. 452(7190), pages 956-960, April.
    5. Nadine Ehmann & Sebastian van de Linde & Amit Alon & Dmitrij Ljaschenko & Xi Zhen Keung & Thorge Holm & Annika Rings & Aaron DiAntonio & Stefan Hallermann & Uri Ashery & Manfred Heckmann & Markus Saue, 2014. "Quantitative super-resolution imaging of Bruchpilot distinguishes active zone states," Nature Communications, Nature, vol. 5(1), pages 1-12, December.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Mami Nakamizo-Dojo & Kenichi Ishii & Jiro Yoshino & Masato Tsuji & Kazuo Emoto, 2023. "Descending GABAergic pathway links brain sugar-sensing to peripheral nociceptive gating in Drosophila," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    2. Aviel Even & Giovanni Morelli & Silvia Turchetto & Michal Shilian & Romain Le Bail & Sophie Laguesse & Nathalie Krusy & Ariel Brisker & Alexander Brandis & Shani Inbar & Alain Chariot & Frédéric Saudo, 2021. "ATP-citrate lyase promotes axonal transport across species," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    3. Michaela Joyce & Federica A. Falconio & Laurence Blackhurst & Lucia Prieto-Godino & Alice S. French & Giorgio F. Gilestro, 2024. "Divergent evolution of sleep in Drosophila species," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    4. Christian Keck & Cristina Savin & Jörg Lücke, 2012. "Feedforward Inhibition and Synaptic Scaling – Two Sides of the Same Coin?," PLOS Computational Biology, Public Library of Science, vol. 8(3), pages 1-15, March.
    5. Hiroyuki Uechi & Kazuki Fukushima & Ryota Shirasawa & Sayaka Sekine & Erina Kuranaga, 2022. "Inhibition of negative feedback for persistent epithelial cell–cell junction contraction by p21-activated kinase 3," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    6. Eyal Rozenfeld & Merav Tauber & Yair Ben-Chaim & Moshe Parnas, 2021. "GPCR voltage dependence controls neuronal plasticity and behavior," Nature Communications, Nature, vol. 12(1), pages 1-11, December.
    7. Yilun Zhang & Tatyana O Sharpee, 2016. "A Robust Feedforward Model of the Olfactory System," PLOS Computational Biology, Public Library of Science, vol. 12(4), pages 1-15, April.
    8. Burak Gür & Luisa Ramirez & Jacqueline Cornean & Freya Thurn & Sebastian Molina-Obando & Giordano Ramos-Traslosheros & Marion Silies, 2024. "Neural pathways and computations that achieve stable contrast processing tuned to natural scenes," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    9. Olga Kubrak & Takashi Koyama & Nadja Ahrentløv & Line Jensen & Alina Malita & Muhammad T. Naseem & Mette Lassen & Stanislav Nagy & Michael J. Texada & Kenneth V. Halberg & Kim Rewitz, 2022. "The gut hormone Allatostatin C/Somatostatin regulates food intake and metabolic homeostasis under nutrient stress," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    10. Jean-Pierre Rospars & Alexandre Grémiaux & David Jarriault & Antoine Chaffiol & Christelle Monsempes & Nina Deisig & Sylvia Anton & Philippe Lucas & Dominique Martinez, 2014. "Heterogeneity and Convergence of Olfactory First-Order Neurons Account for the High Speed and Sensitivity of Second-Order Neurons," PLOS Computational Biology, Public Library of Science, vol. 10(12), pages 1-16, December.
    11. Zachary T. Spencer & Victoria H. Ng & Hassina Benchabane & Ghalia Saad Siddiqui & Deepesh Duwadi & Ben Maines & Jamal M. Bryant & Anna Schwarzkopf & Kai Yuan & Sara N. Kassel & Anant Mishra & Ashley P, 2023. "The USP46 deubiquitylase complex increases Wingless/Wnt signaling strength by stabilizing Arrow/LRP6," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    12. Inga Petelski & Yannick Günzel & Sercan Sayin & Susanne Kraus & Einat Couzin-Fuchs, 2024. "Synergistic olfactory processing for social plasticity in desert locusts," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    13. Tyler R. Sizemore & Julius Jonaitis & Andrew M. Dacks, 2023. "Heterogeneous receptor expression underlies non-uniform peptidergic modulation of olfaction in Drosophila," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
    14. Olga Kubrak & Anne F. Jørgensen & Takashi Koyama & Mette Lassen & Stanislav Nagy & Jacob Hald & Gianluca Mazzoni & Dennis Madsen & Jacob B. Hansen & Martin Røssel Larsen & Michael J. Texada & Jakob L., 2024. "LGR signaling mediates muscle-adipose tissue crosstalk and protects against diet-induced insulin resistance," Nature Communications, Nature, vol. 15(1), pages 1-22, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-38575-6. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.